Response of heat shock protein genes of the oriental fruit moth under diapause and thermal stress reveals multiple patterns dependent on the nature of stress exposure

Abstract

Heat shock protein gene (Hsp) families are thought to be important in thermal adaptation, but their expression patterns under various thermal stresses have still been poorly characterized outside of model systems. We have therefore characterized Hsp genes and their stress responses in the oriental fruit moth (OFM), Grapholita molesta, a widespread global orchard pest, and compared patterns of expression in this species to that of other insects. Genes from four Hsp families showed variable expression levels among tissues and developmental stages. Members of the Hsp40, 70, and 90 families were highly expressed under short exposures to heat and cold. Expression of Hsp40, 70, and Hsc70 family members increased in OFM undergoing diapause, while Hsp90 was downregulated. We found that there was strong sequence conservation of members of large Hsp families (Hsp40, Hsp60, Hsp70, Hsc70) across taxa, but this was not always matched by conservation of expression patterns. When the large Hsps as well as small Hsps from OFM were compared under acute and ramping heat stress, two groups of sHsps expression patterns were apparent, depending on whether expression increased or decreased immediately after stress exposure. These results highlight potential differences in conservation of function as opposed to sequence in this gene family and also point to Hsp genes potentially useful as bioindicators of diapause and thermal stress in OFM.

Thermal limits to survival and activity in two life stages of false codling moth Thaumatotibia leucotreta (Lepidoptera, Tortricidae)

“…The Bogert effect hypothesis predicts that the more mobile adult life stage experiences less selection for plastic responses to thermal environment than the more sedentary larval stage, yet the results of the present study show that the adult stage exhibits a more plastic beneficial response to high temperature stress. This is not altogether surprising because several other studies of Lepidoptera report pronounced beneficial heat hardening responses in the adult stage (codling moth: Chidawanyika & Terblanche, ; oriental fruit moth: Zhang et al ., ). A lack of survival improvement with high temperature shock is, however, not uncommon in Lepidoptera, as in the case of the diamondback moth (Nguyen et al ., ).…”

“…The presence of heat hardening responses without a clear HSP70 response suggests that other macromolecules or adaptive mechanisms may be involved in the survival of T. leucotreta to temperature stress. There are several possible mechanisms worthy of further consideration but perhaps most the important are the small HSPs and ion homeostasis (O'Sullivan et al ., ; Zhang et al ., ), as well as their potential interaction (Armstrong et al ., ), which are increasingly implicated in invertebrate heat tolerance. It remains unlikely that oxygen limitation plays a role in mechanistically governing CT min in larvae (Boardman et al ., ), although it would be useful to consider this hypothesis at high temperatures and across life stages, given that another moth species, Bombyx mori , show strongly divergent stage‐related responses (Boardman & Terblanche, ).…”

Elevated chaperone proteins are a feature of winter freeze avoidance by larvae of the goldenrod gall moth, Epiblema scudderiana

“…This suggests that enhancement of the Hsp70 chaperone and its partner proteins is a conserved component of winter cold hardiness among both freeze tolerant and freeze avoiding goldenrod gall insects. Similarly, elevation of hsp gene expression or HSP protein levels have been associated with cold hardiness in several other insect species (Chen et al, 2006;Rinehart et al, 2006;Yu et al, 2016;Zhang et al, 2016).…”

“…This general elevation of chaperones over the winter may provide several actions that aid insect survival: (1) stabilize/ protect cellular proteins/enzymes from negative effects of cold temperatures and/or rapid temperature change on their conformation and function, (2) extend the half-lives of proteins under environmental conditions where degradation of damaged proteins and resynthesis of new proteins (requiring substantial ATP and fuel expenditures) is not favourable, and (3) contribute to the diapause state by stabilizing proteins over extended periods of hypometabolism. Indeed, elevated amounts of various HSPs are now known to be a feature of diapause in many insect species (Denlinger, 2002;Rinehart et al, 2007;Storey and Storey, 2012;King and MacRae, 2015;Zhang et al, 2016).…”

Sterol glycosyltransferases required for adaptation of Withania somnifera at high temperature

“…A few members of HSPs are the molecular chaperons and essential in maintaining protein degradation, protein folding and activation of proteins involved in signal transduction and control of cell cycle in stress conditions (Wang et al , Zhang et al ). The expressions of HSP genes in the plants are governed by heat shock signaling pathway which is regulated by H 2 O 2 and other ROS, such as NO (Jia et al ).…”